Sucrose ingestion induces Rapid AMPA receptor trafficking

David S. Tukey, Jainne M. Ferreira, Shannon O. Antoine, James A. D'Amour, Ipe Ninan, Soledad Cabeza de Vaca, Salvatore Incontro, Charlotte Wincott, Julian K. Horwitz, Diana T. Hartner, Carlo B. Guarini, Latika Khatri, Yossef Goffer, Duo Xu, Roseann F. Titcombe, Megna Khatri, Dave S. Marzan, Shahana S. Mahajan, Jing Wang, Robert C. FroemkeKenneth D. Carr, Chiye Aoki, Edward B. Ziff

Research output: Contribution to journalArticle

Abstract

The mechanisms by which natural rewards such as sugar affect synaptic transmission and behavior are largely unexplored. Here,weinvestigate regulation of nucleus accumbens synapses by sucrose intake. Previous studies have shown thatAMPAreceptor (AMPAR) trafficking is a major mechanism for regulating synaptic strength, and that in vitro, trafficking of AMPARs containing the GluA1 subunit takes place by a two-step mechanism involving extrasynaptic and then synaptic receptor transport. We report that in rat, repeated daily ingestion of a 25% sucrose solution transiently elevated spontaneous locomotion and potentiated accumbens core synapses through incorporation of Ca2+-permeable AMPA receptors (CPARs), which are GluA1-containing, GluA2-lacking AMPARs. Electrophysiological, biochemical, and quantitative electron microscopy studies revealed that sucrose training (7 d) induced a stable (>24 h) intraspinous GluA1 population, and that in these rats a single sucrose stimulus rapidly (5min)but transiently (<24h) elevated GluA1 at extrasynaptic sites.CPARs and dopamine D1 receptors were required in vivo for elevated locomotion after sucrose ingestion. Significantly, a 7 d protocol of daily ingestion of a 3%solution of saccharin, a noncaloric sweetener, induced synaptic GluA1 similarly to25%sucrose ingestion. These findings identify multistep GluA1 trafficking, previously described in vitro, as a mechanism for acute regulation of synaptic transmission in vivo by a natural orosensory reward. Trafficking is stimulated by a chemosensory pathway that is not dependent on the caloric value of sucrose.

Original languageEnglish (US)
Pages (from-to)6123-6132
Number of pages10
JournalJournal of Neuroscience
Volume33
Issue number14
DOIs
StatePublished - Apr 3 2013

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ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Tukey, D. S., Ferreira, J. M., Antoine, S. O., D'Amour, J. A., Ninan, I., de Vaca, S. C., Incontro, S., Wincott, C., Horwitz, J. K., Hartner, D. T., Guarini, C. B., Khatri, L., Goffer, Y., Xu, D., Titcombe, R. F., Khatri, M., Marzan, D. S., Mahajan, S. S., Wang, J., ... Ziff, E. B. (2013). Sucrose ingestion induces Rapid AMPA receptor trafficking. Journal of Neuroscience, 33(14), 6123-6132. https://doi.org/10.1523/JNEUROSCI.4806-12.2013